Rhythmic coordination and ensemble dynamics in the hippocampal-prefrontal network during odor-place associative memory and decision making
Abstract
Memory-guided decision making involves long-range coordination across sensory and cognitive brain networks, with key roles for the hippocampus and prefrontal cortex (PFC). In order to investigate the mechanisms of such coordination, we monitored activity in hippocampus (CA1), PFC, and olfactory bulb (OB) in rats performing an odor-place associative memory guided decision task on a T-maze. During odor sampling, the beta (20-30 Hz) and respiratory (7-8 Hz) rhythms (RR) were prominent across the three regions, with beta and RR coherence between all pairs of regions enhanced during the odor-cued decision making period. Beta phase modulation of phase-locked CA1 and PFC neurons during this period was linked to accurate decisions, with a key role of CA1 interneurons in temporal coordination. Single neurons and ensembles in both CA1 and PFC encoded and predicted animals' upcoming choices, with different cell ensembles engaged during decision-making and decision execution on the maze. Our findings indicate that rhythmic coordination within the hippocampal-prefrontal-olfactory bulb network supports utilization of odor cues for memory-guided decision making.
Data availability
Data is available for download on figshare:Data DOI: https://doi.org/10.6084/m9.figshare.19620783.v1
-
Rhythmic coordination of hippocampal-prefrontal ensembles for odor-place associative memory and decision makingfigshare, DOI: 10.6084/m9.figshare.19620783.v1.
Article and author information
Author details
Funding
National Institute of Mental Health (R01MH120228)
- Shantanu P Jadhav
National Institute of Mental Health (R01MH112661)
- Shantanu P Jadhav
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Laura L Colgin, University of Texas at Austin, United States
Ethics
Animal experimentation: All experimental procedures were approved by the Brandeis University InstitutionalAnimal Care and Usage Committee (IACUC) and conformed to US National Institutes of Health. Procedures were approved under IACUC Protocol # 21001
Version history
- Preprint posted: June 9, 2020 (view preprint)
- Received: April 17, 2022
- Accepted: December 8, 2022
- Accepted Manuscript published: December 8, 2022 (version 1)
- Version of Record published: December 29, 2022 (version 2)
Copyright
© 2022, Symanski et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,617
- views
-
- 285
- downloads
-
- 12
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
- Stem Cells and Regenerative Medicine
Neural stem cells (NSCs) are multipotent and correct fate determination is crucial to guarantee brain formation and homeostasis. How NSCs are instructed to generate neuronal or glial progeny is not well understood. Here we addressed how murine adult hippocampal NSC fate is regulated and describe how Scaffold Attachment Factor B (SAFB) blocks oligodendrocyte production to enable neuron generation. We found that SAFB prevents NSC expression of the transcription factor Nuclear Factor I/B (NFIB) by binding to sequences in the Nfib mRNA and enhancing Drosha-dependent cleavage of the transcripts. We show that increasing SAFB expression prevents oligodendrocyte production by multipotent adult NSCs, and conditional deletion of Safb increases NFIB expression and oligodendrocyte formation in the adult hippocampus. Our results provide novel insights into a mechanism that controls Drosha functions for selective regulation of NSC fate by modulating the post-transcriptional destabilization of Nfib mRNA in a lineage-specific manner.
-
- Neuroscience
This study investigates the goal/habit imbalance theory of compulsion in obsessive-compulsive disorder (OCD), which postulates enhanced habit formation, increased automaticity, and impaired goal/habit arbitration. It directly tests these hypotheses using newly developed behavioral tasks. First, OCD patients and healthy participants were trained daily for a month using a smartphone app to perform chunked action sequences. Despite similar procedural learning and attainment of habitual performance (measured by an objective automaticity criterion) by both groups, OCD patients self-reported higher subjective habitual tendencies via a recently developed questionnaire. Subsequently, in a re-evaluation task assessing choices between established automatic and novel goal-directed actions, both groups were sensitive to re-evaluation based on monetary feedback. However, OCD patients, especially those with higher compulsive symptoms and habitual tendencies, showed a clear preference for trained/habitual sequences when choices were based on physical effort, possibly due to their higher attributed intrinsic value. These patients also used the habit-training app more extensively and reported symptom relief post-study. The tendency to attribute higher intrinsic value to familiar actions may be a potential mechanism leading to compulsions and an important addition to the goal/habit imbalance hypothesis in OCD. We also highlight the potential of smartphone app training as a habit reversal therapeutic tool.